ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
FIRST REPORT IN THE PERUVIAN AMAZON AND MORPHOLOGICAL DESCRIPTION OF THE
ALIEN SPECIES TRIANCHORATUS ACLEITHRIUM PRIECE & BERRY, 1966 (MONOGENOIDEA:
DACTYLOGYRIDAE) PARASITIZING THE GILLS OF TRICHOPODUS TRICHOPTERUS (PALLAS,
1770) (PERCIFORMES: ANABANTIDAE)
PRIMER REPORTE EN LA AMAZONÍA PERUANA Y DESCRIPCIÓN MORFOLÓGICA DE LA
ESPECIE EXÓTICA TRIANCHORATUS ACLEITHRIUM PRIECE & BERRY, 1966
(MONOGENOIDEA: DACTYLOGYRIDAE) PARASITANDO LAS BRANQUIAS DE TRICHOPODUS
TRICHOPTERUS (PALLAS, 1770) (PERCIFORMES: ANABANTIDAE)
1 Instituto de Investigaciones de la Amazonía Peruana (IIAP), Laboratorio de Parasitología y Sanidad Acuícola, Av. José
A. Quiñones, Km 2.5 – San Juan Bautista, 0784 - Iquitos, Loreto, Perú.
2 Universidad Nacional de la Amazonía Peruana (UNAP), Sargento Lores, 385, Iquitos, Perú
* Corresponding author: germantiss1106@gmail.com
1* 2 2
Germán Augusto Murrieta Morey ; Kevin Morgan Ruíz Tafur ; Edgar Leonardo Dávila Panduro ;
2 2 2
Carlos Tobias Chuquipiondo Guardia ; Carlos Alfredo Tuesta Rojas & José Carlos Zumaeta Cachique
ABSTRACT
Keywords: alien species – monogenoidean – parasite – three spot gourami – Trianchoratus acleithrium – Trichopodus trichopterus
The three spot gourami, Trichopodus trichopterus (Pallas, 1770) is a species native to Southeast Asia
which has been introduced in Peru as a biological controller of vectors of malaria and for ornamentation.
Considering that alien host species may co-introduce their parasites into natural environments, the present
study aims to identify the monogenoideans that parasitize the gills of the three spot gourami, giving a
morphological description of its parasite species and its parasitological indices. Thirty specimens of T.
trichopterus were captured in July 2018 from a natural pond in Iquitos, Peru. Specimens were sacrificed
and then analyzed in the Laboratorio de Parasitología y Sanidad Acuícola of Instituto de Investigaciones
de la Amazonía Peruana (IIAP), Iquitos, Peru. The monogenoidean Trianchoratus acleithrium Priece &
Berry, 1966 was found parasitizing the gills of the three spot gourami T. trichopterus with a prevalence of
30%, 26 parasites collected, with an intensity ranged from 1-12, mean intensity of 2.89 parasites per
infected host and a mean abundance of 0.87 per host.
Neotropical Helminthology
161
Neotropical Helminthology, 2019, 13(2), jul-dic:161-167.
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
Volume13,Number2(jul-dec2019)
Activities associated with trade of non-native
ornamental fish, transport, tourism, and fish farms
for food production are the main means by which
the introduction of exotic fish species and their
parasites occurs around the world (Mendoza-
Franco et al., 2018). Furthermore, the same indus-
tries pose a growing threat to native wildlife if non-
native fishes are later released into the wild (see
Mendoza-Franco et al., 2012).
The three spot gourami Trichopodus trichopterus
(Pallas, 1770) is a species of gourami native to
Southeast Asia. This fish inhabits standing or slow-
moving freshwater and is abundant in Yunnan,
China, Cambodia, Laos, Malaysia, Myanmar,
Singapore, Thailand and Vietnam (Vidthayanon,
2001).
The interest to develop fish culture in the Peruvian
Amazon, as well as the lack of technology for
cultivating native species, determined the need to
introduce species from other countries that already
have proven technology for culturing. In this way,
several species used in pisciculture were
introduced; likewise, other species such as the
three spot gourami T. trichopterus has been
introduced in 1970 as biological control for vectors
of malaria and for ornamentation (Alcántara, 1991;
Ortega et al., 2007).
INTRODUCTION
162
RESUMEN
Palabras clave: especies exóticas – gourami de tres puntos – monogenoideos – parásitos – Trianchoratus acleithrium – Trichopodus trichopterus
Trichopodus trichopterus (Pallas, 1770) es una especie nativa del sudeste asiático que se introdujo en el
Perú como un controlador biológico de los vectores de la malaria y para la ornamentación. Teniendo en
cuenta que las especies hospedadoras exóticas pueden co-introducir sus parásitos en ambientes naturales,
el presente estudio tiene como objetivo identificar los monogenoideos que parasitan las branquias del
gourami de los tres puntos, dando una descripción morfológica de sus especies de parásitos y sus índices
parasitológicos. Treinta especímenes de T. trichopterus fueron capturados en julio de 2018 de un estanque
natural en Iquitos, Perú. Las muestras se sacrificaron y luego se analizaron en el Laboratorio de
Parasitología y Sanidad Acuícola del Instituto de Investigaciones de la Amazonía Peruana (IIAP), Iquitos,
Perú. Se encontró al monogenoideo Trianchoratus acleithrium Priece & Berry, 1966, parasitando las
branquias del gourami de los tres puntos T. trichopterus con una prevalencia del 30%, 26 parásitos
recolectados, con una intensidad que osciló entre 1 y 12, con una intensidad media de 2.89 parásitos por
huésped infectado y una abundancia media de 0,87 por huésped.
In the Peruvian Amazon, the gouramis have
reached the River Nanay, being captured in shallow
areas of the river near the city of Iquitos. Their
presence is significantly high compared to native
species (Alcántara, 1991). Although a systematic
study on species of gourami has not been carried
out yet, it is considered that due to its mere presence
and natural reproduction in the Peruvian Amazon,
its evaluation is warranted. Considering that alien
species may co-introduce their parasites into
natural environments and these may cause
alterations in natural populations of fish species,
the present study aims to identify the
monogenoideans that parasitize the gills of the
introduced three spot gourami, giving a detailed
morphological description of its parasite species
and its parasitological indices.
Thirty specimens of T. trichopterus (Fig. 1) with
5.39 ± 0.38 cm average standard length were
collected in July 2018 from a natural pond located
in the municipality of San Juan Bautista, in Iquitos,
o o
Peru. (3 45 18.73 S / 73 16 40. 72 O). Captured ' '' ' ''
fish were placed into plastic bags and then
transported to the laboratory of “Parasitología y
Sanidad Acuícola” at the the “Instituto de
Investigaciones de la Amazonía Peruana” (IIAP).
Neotropical Helminthology, 2019, 13(2), jul-dic
MATERIAL AND METHODS
Murrieta Morey et al.
163
parasites per infected host and a mean abundance
of 0.87 per host.
The main morphological characteres used for its
identification were: three anchors, being two
posterolateral (ventral anchors) and the other
medial (dorsal anchor); haptoral bars lacking;
copulatory complex composed of a male
copulatory organ and an accessory piece. MCO
tubular, arising from an expanded base, coiled
forming one ring; accesory piece articulated to
cirrus base, a sclerotized rod bifurcate into two
distinct rami, one of which is recurved distally (Fig.
2).
Dactylogyridae Bychowsky, 1933
Trianchoratus Price & Berry, 1966
Trianchoratus acleithrium Price & Berry, 1966
Host: Trichopodus trichopterus (Pallas, 1770)
o o
Locality: Iquitos, Peru. (3 45 18.73 S / 73 16 40. ' '' '
72 O).''
Site in host: Gill filaments
Description (Fig. 3)
Based on 10 specimens – 4 stained, 6 cleared. Body
elongate, 203 – 402 (306; n = 10) long, greatest
width 74 – 154 (104; n = 10) cephalic lobes poorly
developed. Four pairs of head organs lying in
cephalic lobes; cephalic glands not observed. Four
pairs of eyes present, granules elongate ovate,
small. Pharynx muscular, oval; esophagus short;
intestinal caeca two, confluent posteriorly, lacking
diverticula. Peduncle short, narrow; haptor
bilobate 49 – 80 (64; n = 10) long, 63 – 87 (76; n =
10) wide. Three anchors, one dorsal and two
ventral. Dorsal anchor medial, 22 – 27 (25; n = 10)
long, 18 – 23 (21; n = 10) wide, with expanded
superficial root and short deep root; ventral
anchors almost symmetrical, posterolateral, with
well-developed superficial roots and short deep
roots, elongate and curved shaft, and elongate
point. Left ventral anchor, 33 – 42 (39; n = 10) long,
19 – 22 (20; n = 10) wide; right ventral anchor, 33 –
40 (37; n =10) long, 22 – 26 (23; n = 10) wide.
Hooks similar, each with proximal tip with knob
resembling a pin-head, depressed thumb, slightly
curved shaft; 12 – 16 (14; n = 40) long. Testis oval,
dorsal to germarium; germarium elongate; vas
deferens arises from anterior margin of testis,
crosses diagonally along dorsal field of body;
prostatic gland robust, placed dorsal to MCO;
vagina dextral, opens laterally, a sclerotized tube
In the laboratory, fish were measured and then
sacrificed following CONCEA (2013). Later, gill
archers were removed and placed in vials
containing heated water (68 °C). Each vial was
shaken vigorously and 96% ethanol was added.
The content of each vial was examined using a
dissecting microscope and helminths were
removed from the gills or sediment using
dissection needles. Some specimens were cleared
with Hoyer´s medium for their identification based
on the morphology of the sclerotized structures and
others were stained with Gomori´s trichrome
(Humason, 1979; Boeger & Viana, 2006) and
mounted in Dammar gum to determine internal soft
structures.
Sclerotized structures of the species were
photographed with a camera (Axiocam RC 5s)
connected to a microscope (Zeiss Primo Star), and
the images were used to obtain the measurements
of the body, OCM and haptoral sclerites.
Measurements were made following the
procedures of Mizelle & Klucka (1953).
Measurements are in micrometers, using straight-
line distances between extreme points of the
structures measured and are expressed as the range
followed by the mean and number (n) of structures
measured in parentheses. Illustrations were
prepared with the aid of microprojector. The
ecological terms in parasitology followed those
provided by Bush et al. (1997). Voucher specimens
were deposited in the Helminthological Collection
of the Museum of Natural History at the San
Marcos University (MUSM) Lima, Peru (MUSM
3885a-d).
Conflict of interest: The authors declare that they
have no conflict of interest.
Ethical approval: All applicable institutional,
national and international guidelines for the care
and use of animals were followed.
The monogenoidean Trianchoratus acleithrium
Priece & Berry, 1966 was found parasitizing the
gills of the three spot gourami T. trichopterus with a
prevalence of 30%, 26 parasites collected, with an
intensity ranged from 1-12, mean intensity of 2.89
RESULTS
Neotropical Helminthology, 2019, 13(2), jul-dic Trianchoratus acleithrium collected in Peru
164
bearing protruding sclerite, 21 – 26 (24; n = 10)
long. Egg with filament, bell-shaped with slightly
sclerotized walls, 52 – 62 (60; n = 3) long, 28 – 36
(33; n = 3) wide. Vitellaria dense, coextensive with
caeca.
connected to seminal receptacle. Copulatory
complex comprising male copulatory organ
(MCO) and accessory piece. MCO 19 – 25 (23; n =
10) long, consisting of slightly coiled tube with
rounded initial part, grooved accessory piece
Figure 1. Lateral view of Trichopodus trichopterus (Pallas, 1770) captured in the Peruvian Amazon.
Figure 2. Sclerotized structures of Trianchoratus acleithrium Priece & Berry, 1966 from the gills Trichopodus trichopterus
(Pallas, 1770). (1) copulatory complex, (2) dorsal anchor, (3-4) ventral anchors. Bar scale: (1) 20 µm, (2) 15 µm.
Neotropical Helminthology, 2019, 13(2), jul-dic Murrieta Morey et al.
165
Figure 3. (1) Ventral view of Trianchoratus acleithrium Priece & Berry, 1966 from the gills Trichopodus trichopterus (Pallas,
1770), (2) copulatory complex, (3) hook, (4) egg, (5) dorsal anchor, (6-7) ventral anchors. Bar scale: (1) 100 µm, (2) 20 µm, (3) 15
µm, (4) 30 µm, (5) 15 µm.
DISCUSSION introduction of parasites by ornamental fish from
which the consequences of parasite introduction
can be detrimental to native fish. For example,
epizootics that may lead to extensive mortality as
shown for several species of monogenoideans
introduced into farms or aquariums, and from there
to natural populations (Bakke et al., 2002, 2007;
García-Vásquez et al., 2017). Trianchoratus
acleithrium has been cited parasitizing exotic fish
species imported from Asia to different countries,
for example, in T. trichopterus collected in Mexico
(Mendoza-Franco et al., 2018), and in T.
trichopterus collected in Australia (Trujillo-
Gonzáles et al., 2018). Undetected parasites could
present a threat to the profitability and
sustainability of wild environments (Trujillo-
Gonzáles et al., 2018). In the present study, T.
acleithrium is cited for the first time in South
Monogenoideans usually exhibit high host
specificity in comparison with other parasite
groups, parasitizing a single or few closely related
host species (Braga et al., 2014). Trianchoratus
Price & Berry, 1966 was proposed from the gills of
kissing gourami, Helostoma rudolfi (Machan,
1931) captured in Southeast Asia (Price & Berry,
1966). To date, 12 species of Trianchoratus are
identified parasitizing only fish species from Asia
(see Tan & Lim 2009; Chaudhary et al., 2013). In
the present study, T. acleithrium was the only
monogenoidean found in the gills of T.
trichopterus.
There are many reports dealing with the
Neotropical Helminthology, 2019, 13(2), jul-dic Trianchoratus acleithrium collected in Peru
America, being specifically collected in the
Peruvian Amazon. This finding represents an alert,
being necessary future investigations in order to
determine if this parasite is able to parasitize native
fish species and its impacts on natural populations
of fishes.
Phylogenetic dissimilarity of native and alien
fishes is considered an important factor to avoid the
co-invasion of alien monogenoideans (Fletcher &
Whittington, 1998). However, countries with
native fauna phylogenetically similar to exotic fish
species may be at a higher risk of co-introduced
monogenoideans invading native fishes (Lymbery
et al., 2014). In the Peruvian Amazon, fish species
belonging to Perciformes is represented with 8
families, 40 genera and 91 species (Ortega &
Hidalgo, 2008). As T. trichopterus belongs to
Perciformes, T. acleithrium would have the
ability to parasitize species of Perciformes that
cohabit in the same environmets. Studies
concerning to monogenoideans of native fishes
which cohabit in the same places where gouramis
are captured would be necessary to determine if the
alien parasite T. acleithrium is parasitizing native
fish species from the Peruvian Amazon.
We thank the NGO “Amazon Research Center for
Ornamental Fishes” for their assistance in the field
study.
166
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